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Deinococcus Radiodurans  the Consummate Survivor

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Deinococcus Radiodurans  the Consummate Survivor REVIEWS DEINOCOCCUS RADIODURANS THE CONSUMMATE SURVIVOR Michael M. Cox* and John R. Battista‡ Abstract | Relatively little is known about the biochemical basis of the capacity of Deinococcus radiodurans to endure the genetic insult that results from exposure to ionizing radiation and can include hundreds of DNA double-strand breaks. However, recent reports indicate that this species compensates for extensive DNA damage through adaptations that allow cells to avoid the potentially detrimental effects of DNA strand breaks. It seems that D. radiodurans uses mechanisms that limit DNA degradation and that restrict the diffusion of DNA fragments that are produced following irradiation, to preserve genetic integrity. These mechanisms also increase the efficiency of the DNA-repair proteins. 1 IONIZING RADIATION In 1956, Anderson et al. isolated a novel vegetative of genetic tools. Evidence has accumulated for both Any electromagnetic or bacterium from canned ground meat that had been passive and enzymatic contributions to genome res- particulate radiation powerful γ-irradiated at 4,000 Gray (Gy), a dose that is approx- titution (FIG. 1), which provides a framework for our enough to strip electrons from imately 250 times higher than that typically used to discussion in this review. atoms to produce ions. kill Escherichia coli. The authors named this species Micrococcus radiodurans because of its superficial Ionizing-radiation resistance morphological similarity to members of the genus Of all the phenotypes associated with prokaryotes, Micrococcus. However, research on M. radiodurans resistance to ionizing radiation is one of the most dif- over the next 30 years resulted in reclassification of ficult to rationalize in terms of natural selection. As this species and its closest relatives into a distinct there are no naturally occurring environments known phylum within the domain Bacteria2–7. The genus that result in exposures exceeding 400 mGy per year9, name — Deinococcus — was based on the Greek it is unlikely that species evolved mechanisms to adjective ‘deinos’, which means strange or unusual8; protect themselves against the effects of high-dose an apt description for an organism with an ability to ionizing radiation per se. Instead, it seems that the survive genetic damage that sets it apart from much damage introduced by γ-irradiation shares features of the life on Earth. with the damage that results from other stresses to Treatment of Deinococcus radiodurans with high which bacteria have adapted. For example, desicca- *Department of levels of IONIZING RADIATION can produce hundreds tion introduces many DNA double-strand breaks into Biochemistry, University of genomic double-strand breaks TABLE 1, but the the genomes of D. radiodurans10 and members of the of Wisconsin–Madison, genome is reassembled accurately before initiation cyanobacterial genus Chroococcidiopsis11. Both organ- Wisconsin 53706-1544, of the next cycle of cell division. The extraordinary isms are tolerant to desiccation and are resistant to the USA. ‡Department of Biological capacity of Deinococcus spp. to reconstitute their potentially lethal effects of ionizing radiation, which Sciences, Louisiana State genomes has inspired a small but growing commu- might indicate that the radioresistance of these species University and A&M nity of researchers who are interested in the relevant is a fortuitous consequence of their ability to tolerate College, Baton Rouge, mechanisms that are used to achieve this. In recent desiccation-induced strand breaks. Louisiana 70803, USA. Correspondence to J.R.B. years, investigation of the biology and biochemistry of TABLE 2 lists members of six bacterial phyla that are e-mail: [email protected] Deinococcus spp. has accelerated, catalysed by the avail- resistant to ionizing radiation. The Deinococcaceae doi:10.1038/nrmicro1264 ability of genome information and the development are the best-known family on this list, and have been 882 | NOVEMBER 2005 | VOLUME 3 www.nature.com/reviews/micro © 2005 Nature Publishing Group REVIEWS Table 1 | Double-strand breaks formed in E. coli and D. radiodurans is possible that these diverse prokaryotic cells adapted differently to a similar selective pressure and that there Species* Genomes DNA double-strand Average distance per cell breaks‡ at D between lesions might be multiple mechanisms of radioresistance. 37 This latter possibility seems more probable, as fewer Escherichia coli K12 4–5 8–9 530,000 bp independent evolutionary events (the loss of resistance Deinococcus 8–10 275 10,000 bp from each species being considered a separate event) radiodurans R1 would be required to generate the handful of known *In each study, actively growing aerobic cultures were irradiated and the number of double-strand radioresistant species. breaks determined using neutral sucrose-gradient centrifugation. ‡For D. radiodurans this is lesions per unit length of chromosome I (2.64 Mb). Chromosome I is used because it is the largest target Radiation resistance is not restricted to the domain within the cell. Calculations are based on a measured rate of 1 DNA double-strand break per 10 Bacteria. Several HYPERTHERMOPHILIC archaea (members Gray per 5×109 Da of double-stranded DNA. D , the dose at which 37% of the cells survive. 37 of the Euryarchaeota and Crenarchaeota) show extreme ionizing-radiation resistance12–15, in some cases (for studied for five decades. Little has been learnt about the example, Thermococcus gammatolerans) comparable other bacterial species listed, other than their capacity to to that of Deinococcus radiodurans14. tolerate ionizing radiation. Draft genome sequences of Rubrobacter xylanophilus and Kineococcus radiotolerans The Deinococcaceae have been released in the past year, but detailed analyses The Deinococcaceae family comprises 11 validly of these sequences have not yet been reported. described species — D. radiodurans, Deinococcus There is no clear pattern of evolution among proteolyticus, Deinococcus radiopugnans, Deinococcus ionizing-radiation-resistant species (FIG. 2). The scat- grandis, Deinococcus radiophilus, Deinococcus geo- tered appearance of ionizing-radiation resistance thermalis, Deinococcus murrayi, Deinococcus indi- among distinct prokaryotic lineages indicates two cus, Deinococcus frigens, Deinococcus saxicola and possibilities. First, radioresistance could be a ves- Deinococcus marmoris — all grouped in a single genus, tige of DNA-repair mechanisms that were present Deinococcus16–18. Deinococci do not form spores and in ancestral species and have been retained in those are non-motile. Most species grow best in rich media organisms that continue to require this phenotype. at temperatures between 30 and 37oC, with a doubling This explanation assumes that the ancestor’s ability time between 1.5 and 3 hours. However, D. geotherma- to cope with DNA damage has been lost by most lis and D. murrayi are true thermophiles, with optimal descendents, and predicts that the molecular mecha- growth temperatures of 45–55oC. With the exception nisms of radioresistance should be similar among of D. grandis, which is rod-shaped, all Deinococcus spe- ionizing-radiation-resistant species. Second, given cies are spherical cells that exist singly or as pairs and the infrequent occurrence of ionizing-radiation resist- tetrads in liquid culture. ance, it is possible that this phenotype has arisen in To date, D. radiodurans has received more attention unrelated species through horizontal gene transfer, or than the other deinococci. The genome of D. radiodurans possibly convergent evolution. Much as birds and bats strain R1 (ATCC BAA-816) has been sequenced19,20 and evolved wings despite distinct evolutionary origins, it can be accessed at the TIGR Comprehensive Microbial Resource database (see Online links box). The D. radio- durans chromosome is 3.28 Mb, with a GC content of Ionizing radiation 66.6%. There are nine types of short nucleotide repeats, ranging in size from 60 to 215 bp, found at 295 sites DNA double- strand breaks that are randomly scattered in the genome. The genome Mn Mn Mn Mn is segmented and consists of a 2.64-Mb chromosome (chromosome I), a 0.41-Mb chromosome (chromo- some II), a 0.18-Mb megaplasmid and a 0.045-Mb plasmid21. D. radiodurans has between 4 and 10 genome copies per cell, depending on the stage of the bacterial growth phase22,23. γ Mn Mn Repair Mn Mn The -irradiation survival curves of actively grow- Mn ing cultures of D. radiodurans R1 have a shoulder Mn Mn Mn of resistance up to 5,000 Gy24, and until this dose is achieved there is no measurable loss of viability in the irradiated culture. Under these conditions, the D37 dose BOX 1 for D. radiodurans R1 is approximately 6,500 Gy. Assuming that there are eight genome copies per cell in these cultures, a 5,000-Gy dose will introduce Mn Mn Mn Mn approximately 1,600 double-strand breaks per cell. As this dose is sublethal, it can be inferred that potentially Figure 1 | Potential contributions to the recovery from radiation damage in Deinococcus radiodurans. The schematic depicts a D. radiodurans tetracoccus. catastrophic deletions and genome rearrangements The nucleoid in each compartment is highly condensed and maintains its overall architecture occur at low frequencies. Although there is no formal after irradiation. High levels of Mn(II) might contribute to the recovery from DNA damage. proof, it seems that the process of double-strand-break A wide range of enzymes probably also contribute to genome reconstitution.
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